When was brookesia micra discovered

In the years since the original definition of the Brookesia minima group [18] , this group has been usually considered to be monophyletic, although one additional species of comparatively larger size, B. Also, the molecular data have confirmed that B. DNA sequences are now available [14] , [17] and the present study for all described species of Malagasy leaf chameleons except for B. It therefore can be assumed that no other described species of Brookesia will in the future be allocated to the B.

On the contrary, in several other species and species complexes of Brookesia more convoluted taxonomic situations are found. The widespread eastern B. The equally widespread B. Finally, the two morphologically distinct species B.

Amongst leaf chameleons, the miniaturized species of the B. However, somewhat paradoxically, our integrative taxonomic analysis demonstrates that species delimitation and diagnosis is more straightforward in the B.

The concordant and highly supported mitochondrial and nuclear gene trees support the notion that they represent the correct species trees for the Brookesia minima group.

The results are in strong agreement with geographic distribution but indicate homoplasy of morphological traits. The three main groups consistently recovered, named A, B and C in Figs. The nuclear genes furthermore support a position of B. The distribution of species in clade C is surprising at first glance, given that species of this group occur both in eastern rainforests of low- and mid-elevation, and in transitional and dry forests of the west. However, in general terms, niche conservatism seems to have played only a minor role in the diversification of the B.

Such watersheds [43] have been proposed to explain distributional patterns mainly of lemurs, and in fact there are examples from other organisms with a distribution area rather similar to that of clade C of the B.

However, these examples all involve rather recent dispersal events e. The distribution of clade C suggests that opportunities for dispersal across Madagascar's northern-central high plateau have existed either continuously or intermittently for many millions of years via forests associated with rivers flowing both eastwards and westwards from the plateau. The frog sister species pair Boophis luteus east and B. Our well supported molecular phylogeny also provides some insights into the evolution of morphological traits within this group.

Brookesia desperata is deeply nested within clade A and differs in various characters from all other species in this clade: it is larger 25—30 mm vs. Parsimony-optimization of morphological transformations on the molecular tree not shown suggests that the ancestor of clade A did not share these traits. Based on its phylogenetic position in our analysis highly supported by all genes, and by the combined analysis [ Fig. This suggests that the ancestor of B. Such a reversal to a larger body size has also been observed in a miniaturized clade of microhylid frogs of the genus Stumpffia in the same region of northern Madagascar [49] , and in other African frogs [50].

In contrast, clade C consists mainly of rather large-sized species 25—30 mm SVL; Table 3 , and the somewhat smaller size of B. Brookesia micra is morphologically distinct from all other species in the B. At the same time, this is the smallest species of the group, and because short tails and large heads are typically found in juvenile lizards, it is tempting to interpret these traits in B.

However, a clear trend of increasing head size and decreasing tail length with decreasing body length is not evident in the B. For instance, B. And the small-sized B. Phylogenetically, character states for these traits tubercles and spines, head size or tail length do not constitute convincing morphological synapomorphies for any clade or subclade in the B. Genital morphology is useful for species delimitation, and all sister species in the B.

The clade composed of B. On the other hand, both B. This suggests that hemipenial characters might not be particularly useful to reconstruct species-level phylogenies in Brookesia , although they have provided valuable synapomorphies for other major groups within the Chamaeleonidae [51]. Phylogenetic niche conservatism predicts that closely related species will be similar in their ecological niches, and has recently gained attention as a possible factor influencing clade diversification e.

However, within numerous clades of organisms obvious niche conservatism is found at only some, but not all, phylogenetic levels, and this complicates the assessment and analysis of this factor [54].

A detailed analysis of niche conservatism within the B. First, all species of the B. Brookesia tuberculata , from the elevationally diverse Montagne d'Ambre Massif, has only been recorded at — m elevation [5] , [55]. Furthermore, all species in the B. These two species occur at different elevations in a continuous forest block of the Montagne d'Ambre Massif, and their localities are only a few kilometres apart.

Second, despite the apparently narrow ecological tolerance of individual B. The phylogenetic tree indicates recurrent shifts of habitat specialization: for instance, in clade A B.

Similarly, within clade C the mid-altitude rainforest species B. Species of the B. Several species are supposed to occur at multiple localities, e. However, molecular data in these species are so far available from one locality each, and in the cases of B. Given the high degree of genetic divergence among morphologically similar species of the B.

The only species for which molecular data are available from more than one site is B. Microendemism is extreme in the four new species described herein, each of which is known only from its respective type locality. For each of them our analysis includes mitochondrial DNA sequences for a large series of specimens Fig. The high molecular divergences among species thus appear best explained by low vagility and genetic isolation of local populations in these miniaturized species, rather than an exceptionally fast molecular substitution rate.

Only few studies have dealt with individual dispersal and home ranges of chameleons, although movements over relatively long distances have been observed in males of larger chameleon species [56] , [57] , e. No studies have so far tested the possibility of a very low individual dispersal capacity of Brookesia.

In summary, various lines of evidence identify the B. This is suggested by 1 their deep molecular differentiation, with no haplotype sharing among species or populations in nuclear or mitochondrial genes, and concordant phylogenetic signals from independent nuclear and mitochondrial genes, 2 the pattern of regional diversification, with subclades restricted to particular regions of Madagascar, and 3 the presence of consistent differences in external and genital morphology among all species.

We hypothesize that these species have been microendemic to the same small distribution ranges for this extended period of time, with a low prevalence of range shifts, and probably with repeated local extinctions of populations.

It has been noted that most of the 15 Brookesia species in northern Madagascar show a remarkable degree of microendemism [12]. The importance of northern Madagascar has also been assessed based on an explicit analysis of species richness of Brookesia , which was highest in this part of the island [14]. Considering the novel classification and new species of the B. Microendemism is widespread in Malagasy animals, but there are few examples in which it is as extreme as in the miniaturized species of the Brookesia minima group and in frogs of the genus Stumpffia [49].

This indicates a possible body size effect on the degree of microendemism, which is consistent with the body-range size relationship previously demonstrated in the Malagasy mantellid frog radiation [58]. In general, a correlated decrease in species' ranges with decreasing body size is a recognized pattern in animals [59]. A closer analysis of this pattern in Madagascar's biota may yield new insights and provide at least a partial explanation for the prevalence of microendemic patterns in some groups of animals and the absence of such patterns in others.

A previous study found Brookesia from northern Madagascar to be confined almost entirely to rainforest, with only one species, Brookesia stumpffi , also found in the dry forests of the limestone canyons at Ankarana [12]. In addition to these larger leaf chameleon species, three miniaturized species from northern Madagascar B. One miniaturized species, B. In general, in Madagascar, miniaturization of lizards does not appear to be restricted to tropical humid environments.

Dwarf geckos of the genus Lygodactylus occur in montane environments above m elevation and are very common in dry western forests where they can reproduce all year round [60]. Geckos lay eggs with hard calcareous shells that are less prone to desiccation than the soft shells of chameleon eggs.

Smaller body size is correlated with a proportionally higher body surface area and thus higher risk of desiccation, probably even when scales cover the skin, as in squamate reptiles. Given that the climate of Madagascar is characterized by unpredictability at various scales [61] , the presence of miniaturized lizards in dry environments is surprising.

Probably the rather accentuated rainy season even in the west of Madagascar, together with typically low temperatures in the dry season and the humidity buffer provided by leaf litter and fissures in karstic soil provide a microclimate that has allowed these species to survive under superficially adverse conditions. Extremely small animals often display unique behavioural repertoires, and evolutionary novelty may also arise through ecological specialization directly related to size.

For instance, miniaturized frog species specialize in very small prey that often largely consists of mites and ants. Several species from these arthropod groups contain alkaloids, and their consumption may have constituted an important prerequisite for the evolution of skin alkaloid sequestering, aposematic colour and diurnal behaviour in poison frogs [62].

Miniaturized frog species also tend to display derived life history traits [3] with a tendency toward fewer and larger offspring, often correlated with the loss of a free-living, feeding tadpole stage [63]. In snakes and possibly other amniotes, allometry of the body and of organ sizes probably limits the proportion of the body cavity available for the formation of eggs, so that the smallest snakes typically have a rather stout and short body.

Minimum sizes of adult amniotes may therefore be defined by a tradeoff between number and size of offspring [2]. In this study we report a clutch size of two eggs in both B. Several species of larger-sized Brookesia , including B. These findings are consistent with a hypothesis of reduced clutch sizes in miniaturized tetrapods.

Egg length in miniaturized Brookesia is 5. Egg length in larger Brookesia is considerably longer 17 mm in B. However, these comparisons should be interpreted very cautiously, as the size of chameleon eggs often significantly increases after their deposition through intake of humidity, and the reported often anecdotal values might therefore not be directly comparable.

The geckos Sphaerodactylus ariasae and S. Several species of the B. Whether the extreme miniaturization of Brookesia micra can be interpreted as a case of island dwarfism is uncertain. Madagascar as a very large island is well known for several cases of gigantism e. The nocturnal mouse lemurs genus Microcebus include a few species e. Among the amphibians, cophyline microhylids of the genus Stumpffia represent a large radiation with about 40 identified species and candidate species [34] , [49] , [65] , including some of the world's smallest frogs e.

An independent extreme miniaturization event occurred in a still undescribed cophyline genus from southeastern Madagascar [65]. Among chameleons, the species of the B. In this scenario, Madagascar as a large island led to the evolution of the Brookesia minima group whereas the isolated karstic block now representing the islet Nosy Hara, might have favored the extreme miniaturization found in B. Future surveys are needed to clarify whether this species is really endemic to Nosy Hara or more widely distributed.

Considering the available data, which species are actually the smallest vertebrates, amniotes and tetrapods on Earth? If all tetrapods are considered, the record clearly belongs to the anurans. However, identifying which is the smallest species is futile and strongly depending on the measuring scheme. All species competing for the title of smallest frog and thus smallest tetrapod in the world Eleutherodactylus iberia , Brachycephalus didactylus , Stumpffia pygmaea , S.

Among amniotes, the smallest species are lizards, but they are consistently larger than amphibians, suggesting that different constraints are acting on this group. The maximum recorded SVL of Sphaerodactylus ariasae 18 mm is below the maximum value in Brookesia micra However if using TL as yardstick, the record of the smallest squamate and amniote in fact applies to B. Iincluding morphological determination key, Table S1 voucher specimens and Genbank accession numbers , Table S2 divergence-date calibration priors , Table S3 additional morphometric measurements , Table S4 additional morphological data , Figure S1 chronogram , Fig.

S3 holotype of B. S4 holotype of B. S5 holotype of B. S6 holotype of B. Anne Yoder provided tissue samples. Jan van Arkel prepared the Brookesia minima hemipenis photograph. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract Background One clade of Malagasy leaf chameleons, the Brookesia minima group, is known to contain species that rank among the smallest amniotes in the world.

Introduction Extremes in nature such as gigantism and dwarfism in organisms attract considerable attention from the general public, but also allow biologists to gain general insights into morphological and ecological constraints.

Materials and Methods Several study sites in northern Madagascar including rainforests and deciduous dry forests on karstic limestone were surveyed for reptiles in the period between and Nomenclatural Acts The electronic version of this document does not represent a published work according to the International Code of Zoological Nomenclature ICZN , and hence the nomenclatural acts contained in the electronic version are not available under that Code from the electronic edition.

Results New locality records of diminutive leaf chameleons During intensive fieldwork in northern Madagascar, we discovered numerous new populations of leaf chameleons of the Brookesia minima group Fig. Download: PPT. Figure 1. Map of northern Madagascar showing distribution of species of the Brookesia minima group. Molecular phylogeny and molecular differentiation Sequences from the northern populations described herein form strongly supported clades that are deeply divergent from each other and from the remaining Brookesia species Fig.

Figure 2. Phylogenetic relationships among species of the Brookesia minima group based on mitochondrial DNA sequences. Morphological and morphometric differences Despite their superficial similarity, a detailed comparison yielded numerous differences in morphology among species in the B.

Figure 4. Morphometric differentiation among species of the Brookesia minima group. Table 1. Morphometric measurements in mm of examined type specimens of Brookesia tristis and B. Table 2. Morphometric measurements in mm of examined type specimens of Brookesia micra and B. Table 3. Brookesia micra is one of four new species of chameleon they documented on their expedition to Madagascar, which according to The Local is home to nearly half of the world's known species of the reptile. The country is known for its many rare species of giants — including giant lemurs and tortoises — as well as dwarfs, such as the world's smallest primate, the mouse lemur, and some of the tiniest known frogs.

Brookesia micra , too, shares the island with the world's largest chameleons , which can grow to almost 70 centimeters long. This is why, during the day, they were observed to flee when the leaf litter they were in was disturbed. In these cases, the animals roll on their side and tuck their limbs in so that they look like a dead leaf.

These little chameleons are active during the day diurnal and sleep on low branches of bushes during the night. Chameleons are not the cuddliest animals, it seems! Like other chameleons, Brookesia also reproduce by laying eggs. The female digs a small hole and disposes of eggs three to six weeks after copulation. The young hatch about three months after the eggs have been laid.

By now, there are 30 subspecies of Brookesia that are recognized as valid. Almost half of them are known from single localities, which shows that this species of chameleon prefers a small range with very specific conditions of climate and environment.

The highest number of them can be found in northern Madagascar. Scientific names are usually complicated, which is why most people avoid them when talking about animals or plants. Unfortunately, Brookesia micra has no name aside from its scientific classification — maybe we just do not talk about it enough! The species name Brookesia is in honor of the British naturalist Joshua Brookes who lived between and Rosa is a German-Canadian writer, a PhD student of English literature, and an amateur natural science enthusiast.

When the Gondwana supercontinent split apart million years ago, these lonely survivors were isolated on islands that would one day become New Zealand,.

Alligators and crocodiles in general are some of the most feared animals in the world. Reptiles are a group of animals that breathes air and has scales instead of hair or feathers. All four species belong to the genus Brookesia , which already had some very small species, with members resembling juveniles of larger species. However, there is a tinier dwarf gecko found in the British Virgin Islands. All of the leaf chameleons look extremely similar, so researchers had to revert to genetic analysis to determine if they belonged to separate species.